The
worldwide maintenance of the honeybee has major ecological, economic,
and political implications. In the present study, electromagnetic waves
originating from mobile phones were tested for potential effects on
honeybee behavior. Mobile phone handsets were placed in the close
vicinity of honeybees. The sound made by the bees was recorded and
analyzed. The audiograms and spectrograms revealed that active mobile
phone handsets have a dramatic impact on the behavior of the bees,
namely by inducing the worker piping signal. In natural conditions,
worker piping either announces the swarming process of the bee colony or
is a signal of a disturbed bee colony.
Keywords
worker bee acoustic communication mobile phone handset worker piping induction
Honeybees
are essential partners for the success of agriculture. The economical
role of honeybees in worldwide pollination has been valued to be around
153 billion euros in the year 2005 (Gallai et al. 2009). Bee losses have been recorded for more than a century (Hart 1893; Aikin 1897; Beuhne 1910; Wilson and Menapace 1979).
Scientists suspect many factors to be responsible for the killing of
the bees, of which the varroa mite, pesticides, viruses, farming
practices, monoculture, hygiene in the hive, and climatic factors are
the most widely cited possibilities. Starting in 2003–2004, bee colonies
worldwide suddenly began to show symptoms of the so-called colony
collapse disorder (CCD). CCD initially affects the worker bees, which
desert the hive. The queen bee is usually abandoned in the hive with the
young brood and with an abundance of honey, so that the colony can
survive for a very short time. However, without the worker bee
population, the colony becomes unsustainable and dies out. Never before
have honeybees disappeared globally and at such a high rate.
Current
theories about the potential cause(s) of CCD essentially include
increased losses due to the invasive varroa mite (Donzé et al. 1998).
Pesticide poisoning (through exposure to pesticides applied for crop
pest control), potential immune-suppressing stress on bees (caused by
one or a combination of several factors such as apiary overcrowding,
pollination of crops with low nutritional value, pollen or nectar
dearth), drought, monocultural practices, migratory stress (brought
about by the moving of the bees in long distances), and increased
transmission of pathogens have also been usually cited as a cause of CCD
(U.S.D.A. 2007). Other causes might include genetically modified crops (Malone and Pham-Delegue 2001) and exceptionally cold winters.
Recent
efforts have been made to study another potential cause responsible for
bee losses: man-made electromagnetic fields. The results obtained to
date have been highly controversial. In princeps
studies performed by using digitally enhanced cordless telephones
located in the bottom of beehives, it has been shown that exposed
honeybees were perturbed in their returning behavior to the hive after
foraging (Harst et al. 2006; Diagnose-Funk 2007; Stever et al. 2007).
Honeybees possess magnetite crystals in their fat body cells and they present magnetic remanence (Gould et al. 1978; Keim et al. 2002). These magnetite structures are active parts of the magnetoreception system in honeybees (Hsu and Li 1994; Hsu et al. 2007).
Honeybees can be trained to respond to very small changes in the
constant local geomagnetic field intensity (Walker and Bitterman 1989a). They can also communicate through chemical and acoustical means (Winston 1991; Tautz 2008).
Therefore, the analysis of the sound features of bee colonies was a
method of choice in the present study, since it can be correlated with
the activity of the bees (Esch 1967; Michelsen et al. 1986; Donahoe et al. 2003; Pierce et al. 2007; Ferrari et al. 2008).
To
my knowledge, no systematic studies have been conducted on potential
effects of electromagnetic radiation from mobile phones on honeybee
behavior. Here, I present results from corresponding original
experiments I have carried out with honeybee populations exposed to
active mobile phone radiation. The goal of these experiments was to
identify potential effects of mobile phone communications on honeybee
behavior and to establish simple methodology to enable other beekeepers
to reproduce the experiments.
2 Materials and methods
2.1 Sound recording and analysis
An
acoustical method based on sound analysis for classification was
employed to identify the changes triggered by mobile phone handsets on
the behavior of the honeybee Apis mellifera carnica.
The sounds produced by the bees in their normal activities were
recorded as negative control (with or without inactive mobile phones in
the hive); activity of the bees was also recorded with active mobile
phones in the hive (see below). Five healthy hives (either Dadant-Blatt
or Swiss Bürki types) were monitored for sound during several recordings
performed between February and June 2009. During the previous autumns
and winters, the bees had been treated against the varroa mite Varroa destructor with formic acid and oxalic acid, as recommended elsewhere (Charrière et al. 2004).
Beehives were located either in the beekeeping and apiary school of the
city of Lausanne (altitude, 749 m) or in a second site used by
beekeepers north of the city of Morges (altitude, 510 m; both locations
in Switzerland). The recording device consisted of a bidirectional
compact microphone (Olympus ME-31) with frequency response from 70 to
14,000 Hz connected to a vocal recorder (Olympus LS-10). The use of
omnidirectional microphones such as the ECM 3005 (Monacor) or the
electret condenser 33-3013 (Radio Shack) is also possible, as described
elsewhere (Ferrari et al. 2008; Rangel and Seeley 2008).
The recorded signal was digitized as a Waveform audio file format sound
file with 160 kbps. The computer program Adobe Audition 1.5 was
employed for the manual analysis of the sound files and for the
generation of the audiograms (also called sonograms) and spectrograms
(oscillograms), as described elsewhere (Ferrari et al. 2008).
In
this pilot study, more than 80 different sound recordings were
performed in five different hives throughout the assay period starting
early February and ending June 2009. In the geographic area where the
experiments took place, the bees usually begin to forage to collect
nectar and pollen in early March, depending on the weather conditions.
Sounds
made by honeybees were recorded in the two conventional models of hives
(Swiss Bürki and Dadant-Blatt) that are found in Switzerland.
2.2 Mobile phone experimental arrangement
Two
mobile phone handsets were randomly chosen from a selection of four
different apparatus having specific energy adsorption rate (SAR) values
of either 0.271, 0.62, 0.81, or 0.98 W/kg (tissue) and 900 MHz GSM
roaming (Global System for Mobile communications, originally from Groupe Spécial Mobile).
The sum of the two random SAR values was always below the 2-W/kg
maximum upper limits recommended in the guidelines of the International
Commission on Non-Ionizing Radiation Protection (I.C.N.I.R.P 1998). Four different subscriber identity module cards unrelated to the experimenter were randomly used.
For
negative controls, the two apparatus were not present in the hive
during the recording of the natural background sounds made by the bees.
For undisturbed control experiments (“sham” experiments), the two mobile
phone handsets were either shut down or kept in the standby mode. The
basic setup of the experiments is schematically shown in Figure 1.
Apparatus positioning in the different hives. a Schematic drawing. Sound recorder 1 was connected to a microphone 2, the latter was placed in the close vicinity of the bees in the hive. The first (emitting) mobile phone 3 was connected with hands-free kit, the latter having its small microphone maintained on the loudspeaker of a radio apparatus 4. A second (receiving) mobile phone 5,
also having a hands-free kit, was also kept inside the hive. The use of
the radio apparatus is intended to allow a permanent communication
between the two mobile phone handsets, in order to avoid unwanted
disconnection after a while. b Image of a Dadant-Blatt model of beehive. The microphone is placed through the upper nourishing hole. c
Image of a Swiss Bürki model of beehive. The microphone was placed
behind a board having a grid instead of a glass plate. During the
experiments, the door of the Bürki hive was closed and the Dadant-Blatt
hive was covered with the roof. A similar positioning can be easily
performed with other types of beehives.
In
order to establish whether inactive mobile phone handsets perturbed the
behavior of the bees, two mobile phone handsets were placed in the hive
in close vicinity of the honeybees. In a first series of experiments
(negative control; n = 8), two
inactive (“off” mode) mobile phone handsets were placed in the hive for
up to 24 h. In a second series of experiments (sham experiments,
“standby” mode; n = 10), the two
mobile phone handsets were kept in the hive in the standby mode, for
prolonged periods of time (4 to 24 h). As positive control experiments,
the two mobile phone handsets were employed in an active communication
mode. The first mobile phone was placed in the hive and was supplemented
with a hands-free kit, the mini microphone of which was held in front
of a radio apparatus maintained outside the hive (≈60 cm away, so that
it does not interfere with the recording performed by the microphone
near the bees) and constantly playing the France info program (output of
the small radio loudspeaker, −18 ± 2 dB at 1 cm). This enables a
permanent signal to be sent from this first to a second telephone,
otherwise without this signal the communication is automatically
interrupted after a period of time. To generate a mobile phone
communication near the bees, the first mobile phone was triggered to
call a second mobile phone that was also placed in the hive. The
communication was established after a ringing signal lasting from 5 to
10 s. This second apparatus was also supplemented with a hands-free kit.
The sum of the SAR values of the two mobile phones was always below the
recommended limit of 2 W/kg, as mentioned above. Several independent
experiments (n = 12) with the
presence of actively communicating mobile phone handsets in the hive
were performed. The established active mobile phone communication could
be controlled at any time in two different ways: by direct hearing of
the communication using the hands-free kit from the second mobile phone,
or by controlling the functional state of the communication by
calling—from a third independent telephone—one of the two active mobile
phone handsets involved in the experiment.
For each
experiment, local weather parameters (temperature, wind, precipitation,
atmospheric pressure, and duration of sunshine) were obtained from the
Office Fédéral de Météorologie et de Climatologie (MétéoSuisse).
3 Results
3.1 Background control experiments
The
analysis of the sound files revealed similar characteristics and events
that were not dependent on the model of the beehive (Figure 2).
Beehives undisturbed by a mobile phone apparatus revealed the same
sound characteristics as previously reported for other honeybee colonies
(see “Discussion”). The fundamental frequency of A. mellifera carnica
was in the range of 450 to 500 Hz. Slightly less activity of the bees
was recorded during the night than during the day. More sound
intensities were recorded during spring and early summer than during
winter, thus probably reflecting the number of the active bees present
in the hives.
Spectrograms and audiograms of hive sounds. a, c Swiss Bürki model. b, d Dadant-Blatt model. a, b without any mobile phones in the hive. c, d
with two mobile phones kept in standby mode in the hives. Intensity
values of audiograms might vary between beehives, depending on the
microphone positioning and the number of bees in the undisturbed hive.
Spectrograms are reported in hertz (Hz); audiograms are normalized (n.a. −1 to +1). Time (t) is indicated in minutes
3.2 Mobile phone handsets in standby mode in the hive
The
analysis of the various sound files revealed that the bees were not
disturbed by these inactive or standby mobile phone handsets, since no
dramatic changes in the fundamental intensity and frequency patterns of
the sounds produced in the hive were recorded (Figure 2c, d), as compared to the background experiments performed without any mobile phone handsets (Figure 2a, b).
3.3 Mobile phone handsets activated in the hive
A result from a typical sound recording experiment is shown in Figure 3a.
Mobile phone handsets in the hive were initially kept for a while
(around 25 min) in standby mode and then put in an active communication
mode. Sound analysis in the beehive revealed that the bees initially
remained calm after the onset of the communication mode, but started to
produce sounds that were higher in both frequency and amplitude after
about 30 min of communication of the mobile phone handsets. After about
15 additional minutes, the mobile phone handset communication was
interrupted. The bees returned to a quiet state after 2 to 3 min, since
the frequency and intensity in the hive had returned to the basal values
recorded in the beginning of the experiment. Negative control runs
showed that the radio itself did not induce any changes in bee behavior
with mobile handsets deactivated.
Induction of honeybee worker piping by mobile phone handsets. a standby mobile phone handsets in the hive were activated 25 min. after the onset of the experiment (1). The beginning of increased noise and frequency in the hive was observed ca. 35 min later (2) and is indicated by a longer arrow. The cessation of the mobile phone communication is indicated (3). b
Recording of bee noise in a hive submitted to prolonged (20 h) active
mobile phone handsets. Spectrograms are reported in hertz (Hz); audiograms are normalized (n.a. −1 to +1). Time (t) is indicated in minutes.
In
order to assess how much time the bees would need to return to a basal
sound status after mobile phone communication, experiments were
performed by placing in the hive actively communicating mobile phone
handsets for prolonged periods of time ranging up to 20 h. Sound
analysis revealed that the bees’ sound values increased in both the
intensity and amplitude ranges throughout the experimental period, as
compared to background values prior to onset of the mobile phone
communication. In each of the independent experiments, both the sound
intensity and the frequency increased about 25 to 40 min after the onset
of the mobile phone communication. Twelve hours after the cessation of
the mobile phone communication in the hive, the bees were still
producing more sound in both intensity and frequency as compared to the
initial background mode, suggesting that the behavior of the bees
remained perturbed for up to 12 h after the end of a prolonged mobile
phone communication. Analysis of a shorter period of time lasting 3 min
is presented (Figure 3b).
When
the sound produced by honeybees in hives containing active mobile phone
handsets was analyzed in more detail, it was determined that the bees
were producing the so-called “worker piping” (Figure 4a).
Spectrograms obtained in the present study revealed various modes of
worker piping. First, bimodal pipes having a fundamental frequency of
around 150–250 Hz and a duration of about 200 ± 51 ms (n = 60 pipes) and 430 ± 103 ms (n = 30
pipes) were recorded throughout the experiment involving mobile phone
handsets communication in the hive. The harmonic nature of each pipe, as
compared to results presented elsewhere (Seeley and Tautz 2001),
was also evident. Another shorter type of worker piping, having a
fundamental frequency of around 400–500 Hz and a duration of about
9 ± 2 ms (n = 50 pipes), was also recorded as a prolonged succession of pulses lasting together up to 2 s (Figure 4b).
This short piping signal was also presenting harmonic features ranging
up to several thousand hertz. Two other types of signals were also
recorded; however, less often than the two signals described above, a
strong harmonic piping signal with a basal frequency of 500 ± 50 Hz and
lasting 75 ± 15 ms (Figure 4c; n = 10) and a signal with a basal frequency of around 2,250 ± 250 Hz and lasting 225 ± 50 ms (n = 10; Figure 4d). Analysis of some recordings presented a mixture of the signals mentioned above (Figure 4e).
All these different signals were recorded solely in beehives that were
subjected to the influence of actively communicating mobile phone
handsets, irrespective of both the location and the season when the
experiments were performed. Moreover, the observations of worker piping
were also independent of the weather conditions prevailing during the
experiments.
Mobile phone-induced honeybee worker piping. Various modes of worker piping (a–e)
were recorded in the presence of actively communicating mobile phone
handsets in the hive. Spectrograms are reported in hertz (Hz); audiograms are normalized (n.a. −1 to +1). Time (t) is indicated in seconds.
4 Discussion
The
results of the present pilot study clearly show that the presence of
actively communicating mobile phone handsets in the close vicinity of
honeybees had a dramatic effect, namely the induction of worker piping
which was regularly observed about 25 to 40 min after the onset of the
mobile phone communication. This observation means that: (1) honeybees
are sensitive to pulsed electromagnetic fields generated by the mobile
telephones and (2) under these circumstances, observable changes in the
behavior of the bees are not artificial, but can be proven to occur
reproducibly. Although mobile phones are not present in the close
vicinity of honeybees in real life, this study provides elements for the
establishment of further experiments involving such apparatus placed at
increasing distances from the bees. Potential consequences of these
observations are discussed below in more detail.
4.1 Rationale of the experimental design
The
experimental design employed was set up in order to enable beekeepers
and researchers in the field to easily reproduce the experiments with
the use of conventional materials and user-friendly computer programs.
Honeybees are usually not living in the close vicinity of
electromagnetic fields induced by mobile phone handsets in the hive.
However, the conditions employed in the present experiments have
biological significance, since the sum of the SAR values from the two
mobile phone handsets were always below the 2-W/kg maximal value
recommended for this frequency (I.C.N.I.R.P 1998).
It seems likely that a similar effect on bees can occur with relatively
low-dose exposure over a prolonged period of time. In this context, it
should be emphasized that radio frequency electromagnetic fields
(RF-EMF) have increased by an order of magnitude over the last 20 years
in Switzerland; a mean weekly exposure of 0.13 mW/m2 (83.8% of all emitting RF-EMF) has been reported (Frei et al. 2009).
Since both randomly visited outdoor locations and the proximity to
mobile phone base stations showed a mean RF-EMF exposure of 0.21 mW/m2,
experiments employing two mobile phone handsets in the hive were
finally chosen for practical reasons. The experiments described in this
article might therefore be applicable everywhere, since nearly all
countries in the world today are readily covered with GSM networks (GSM
roaming, coverage maps).
4.2 Mobile phone handsets and induced honeybee worker piping
It
is known that honeybees possess magnetite crystals in their fat body
cells and that they present magnetic remanence (Gould et al. 1978; Keim et al. 2002). These magnetite structures are active parts of the magnetoreception system in honeybees (Hsu and Li 1994; Hsu et al. 2007).
Importantly, it has been shown that honeybees can be trained to respond
to very small changes in the constant local geomagnetic field intensity
(Walker and Bitterman 1989a).
In that study, magnetic anomalies as low as 26 nT (nanoTesla) were
responsible for changes in the foraging behavior. Moreover, attached
magnets impair magnetic field discrimination by honeybees (Walker and
Bitterman 1989b).
Therefore, it remains to be established which minimal level in
variations of the local pulsed electromagnetic fields induced by mobile
phone handsets and base stations might trigger changes in the bees’
behavior, such as the induction of honeybee worker piping shown here. It
is known for several decades that worker piping is associated with
disturbance of the hive by, for example, intruders or jarring (Wenner 1964).
The latter author recorded sounds that were called “croaking” and
“bipping.” This may present one explanation for the present observations
assuming that mobile phone handsets triggered disturbances in the hive
in a similar way (see Figure 4).
The
experiments presented in this pilot study should be reproduced in hives
totally protected or not with additional copper or aluminum Faraday
cages. Additional clues for the ferromagnetic transduction hypothesis
(Kirschvink and Gould 1981)
and a plausible mechanism for the sensitivity of honeybees to localized
electromagnetic anomalies might therefore be obtained. Such behavioral
changes cannot only be analyzed at the behavioral level with sound
analysis, but also at the molecular level by studying the gene
expression profiles using microarrays, as it was done for the
infestation of honeybees with the varroa mite (Navajas et al. 2008).
Although worker piping can be associated with foraging in undisturbed queenright colonies of honeybees (Pratt et al. 1996), it is usually a signal that is produced shortly before takeoff of a swarm (Seeley and Tautz 2001; Rangel and Seeley 2008).
Worker piping in a bee colony is not frequent, and when it occurs in a
colony, that is not in a swarming process, no more than two bees are
simultaneously active (Pratt et al. 1996).
The induction of honeybee worker piping by the electromagnetic fields
of mobile phones might have dramatic consequences in terms of colony
losses due to unexpected swarming. The present study suggests that
active mobile phone handsets in beehives noticeably induce the rate of
worker piping. However, no evidence for piping of the laying queen (see
Schneider and Lewis 2004) was observed.
In
the present study, no swarming process was initiated after 20 h of
exposure to mobile phone handsets, even though the piping signal was
observed. It should therefore be hypothesized that although the piping
signal is serving as a primer for swarm exodus other modalities and/or
signals (e.g., the shaking and buzz-run signals or chemical components)
may be required in the complex swarming process (Rangel and Seeley 2008). The “buzz-run” or “Schwirrlauf”
rate is perhaps the required crucial signal that appears 15 min before
the massive exodus of honeybees during the swarm departure process
(Seeley and Tautz 2001; Rangel and Seeley 2008).
Moreover, it might be possible that a more prolonged exposure
(>20 h) of the honeybees to the actively communicating mobile phone
handsets is required for the complete induction of the swarming process.
Recently, a study suggested that cell phones and cellphone towers near
beehives interfere with honeybee navigation: in one experiment, it was
found that when a mobile phone was kept near a beehive it resulted in
collapse of the colony in 5 to 10 days, with the worker bees failing to
return home, leaving the hives with just queens, eggs and hive-bound
immature bees (Sahib Pattazhy 2009).
To minimize harm to the bees, it was decided to limit their continuous
exposure to mobile phone communications to a maximum of 20 h in the
present study.
Further confirmation of the current
results and their implications regarding a direct correlation between
erratic honeybee behavior and mobile phone-generated electromagnetic
fields would substantiate one more explanation for the “disappearance”
of bee colonies around the world. This phenomenon accounts for 43% of
all bee losses, apart from overwintering (39%), mite disease, (15%) and
pesticides (3%) as recently described in a national survey performed in
the United States (Bee Alert Technology 2007).
Experiments should be undertaken to establish the correlation between
the time necessary for the onset of worker piping and the intensity of
the electromagnetic fields present in the vicinity of the beehive. For
future experiments, in complement to the present original study and in
order to reach more “natural” conditions, mobile phone apparatuses
should be placed at various increasing distances away from the hives.
Video recordings showing the modifications in the bees’ behavior in the
hive should also be performed.
Notes
Acknowledgements
This
work was performed under the full responsibility of the main author
(D.F.). I thank Prof. Jürgen Tautz for his scientific expertise, Prof.
Harald Berresheim and Dr. David Hacker for the critical reading of the
manuscript, Michel Roth for providing the opportunity to perform
experiments in the apiary school of Lausanne, Dr. Jacques-Henri
Penseyres and Pierre-André Bonzon for their interest in future
experimental projects, the late Philippe Hug (to whom this scientific
article is dedicated) and Peter Loepfe for helpful comments, and the
beekeepers in the apiary clubs of Lausanne and Morges for their
collaboration and scientific interest.
Son émis par les ouvrières en réaction à la proximité d'un téléphone portable
Ouvrière / communication accoustique / téléphone portable / stimulus
Mobiltelefon induzierte Piepstöne von Arbeiterinnen der Honigbiene. In
den letzten Jahren häufen sich Berichte über einen weltweiten Schwund
an Honigbienen in Folge einer Völkerverlustkrankheit (colony loss
disease, CCD), bei der Völker massiv und plötzlich eingehen, ohne dass
es vorhergehende Anzeichen einer Krankheit oder Parasitenbefall gibt.
CCD hat schwerwiegende Auswirkungen für den Anbau vieler Früchte und
Gemüse, die auf Bestäubung durch Insekten angewiesen sind Milbenbefall,
Pestizide, eine reduzierte Immunität, bakterielle und virale
Infektionen, genetisch modifizierte Feldfrüchte und Anbaupraktiken
stehen im Verdacht, eine Rolle beim Schwund der Bienenvölker zu spielen.
Berichten in wissenschaftlichen und allgemeinen Medien zufolge besteht
auch die Möglichkeit, dass Mobiltelefone hierzu beitragen können, da
Bienen Schwierigkeiten bei der Heimfindung hatten, wenn Basisstanionen
für schnurlose Telefone unter den Völkern installiert waren. Mikrowellen
könnten demzufolge einen Teil der Verantwortung für das CCD-Syndrom
tragen. In dieser Arbeit untersuchte ich die potentiellen Effekte von
konventionellen Mobiltelefonen produzierten elektromagnetischen Feldern
auf Honigbienen. Hierzu wurden zwei Geräte im aktiven Modus und mit
einer Summe an spezifischen Energieabsorptionsraten unterhalb der
offiziellen internationalen Maximalwerte (2 Watt pro Kilo Gewebe) in der
Nähe von Bienen aufgestellt und die von Bienen produzierten Piepstöne
aufgezeichnet und analysiert. Dies zeigte, dass sich Bienen durch die
aktiv kommunizierenden Mobiltelefone im Volk gestört fühlten und zum
Senden von Piepstönen angeregt wurden. Unter natürlichen Bedingungen
sind solche Piepstöne ein Signal für die Schwarmvorbereitung oder eine
Reaktion auf Störungen im Volk. Das Senden von Piepstönen setzte nicht
sofort nach Einschalten der Mobiltelefone ein, sondern erst nach 25 bis
40 Minuten. Diese Beobachtungen weisen darauf hin, dass die Bienen für
pulsierende elektromagnetische Felder empfänglich sind und sensibel auf
Verhaltensänderungen reagieren. Ein Schwund an Bienenvölkern wird v.a.
in Erdteilen beobachtet (Nordamerika, Europa, Australien, Südbrasilien,
Taiwan und Japan), in denen Mobiltelefone weit verbreitet sind. Es
stellt sich daher die Frage, ob der Zusammenhang von CCD und einer
intensiven Nutzung von Mobiltelefonen noch als reine Spekulation
angesehen werden kann.
This
article is distributed under the terms of the Creative Commons
Attribution Noncommercial License which permits any noncommercial use,
distribution, and reproduction in any medium, provided the original
author(s) and source are credited.
References
Aikin, R.C. (1897) Bees evaporated: a new malady. Glngs. Bee Cult. 25, 479–480Google Scholar
Donahoe, K., Lewis, L.A., Schneider, S.S. (2003) The role of the vibration signal in the house-hunting process of honey bee (Apis mellifera) swarms. Behav. Ecol. Sociobiol. 54, 593–600CrossRefGoogle Scholar
Donzé,
G., Fluri, P., Imdorf, A. (1998) A look under the cap: the reproductive
behaviour of Varroa in the capped brood of the honey bee. Am. Bee J. 138, 528–533Google Scholar
Esch, H. (1967) Sounds produced by swarming honey bees. J. Comp. Physiol. A. 56, 408–411Google Scholar
Ferrari,
S., Silva, M., Guarino, M., Berckmans, D. (2008) Monitoring of swarming
sounds in bee hives for early detection of the swarming period. Comput.
Electron. Agric. 62, 72–77CrossRefGoogle Scholar
Frei,
P., Mohler, E., Neubauer, G., Theis, G., Bürgi, A., Fröhlich, J.,
Braun-Fahrländer, C., Bolte, J., Egger, M., Röösli, M. (2009) Temporal
and spatial variability of personal exposure to radio frequency
electromagnetic fields. Environ. Res. 109, 779–785PubMedCrossRefGoogle Scholar
Gallai,
N., Salles, J.M., Settele, J., Vaissière, B.E. (2009) Economic
valuation of the vulnerability of world agriculture confronted with
pollinator decline. Ecol. Econ. 68, 810–821CrossRefGoogle Scholar
Gould, J.L., Kirschvink, J.L., Deffeyes, K.S. (1978) Bees have magnetic remanence. Science 201, 1026–1028PubMedCrossRefGoogle Scholar
Harst,
W., Kuhn, J., Stever, H. (2006) Can electromagnetic exposure cause a
change in behaviour? Studying possible non-thermal influences on honey
bees—an approach within the framework of educational informatics. http://agbi.uni-landau.de/material_download/IAAS_2006.pdf. Accessed 15 Sept 2009
Hsu, C.Y., Ko, F.Y., Li, C.W., Fann, K., Lue, J.T. (2007) Magnetoreception system in honeybees (Apis mellifera). PLoS. ONE 2, e395PubMedCrossRefGoogle Scholar
I.C.N.I.R.P
(1998) Guidelines for limiting exposure to time-varying electric,
magnetic, and electromagnetic fields (up to 300 GHz), International
Commission on Non-Ionizing Radiation Protection. Health. Phys. 74, 494–522Google Scholar
Keim,
C.N., Cruz-Landim, C., Carneiro, F.G., Farina, M. (2002) Ferritin in
iron containing granules from the fat body of the honeybees Apis mellifera and Scaptotrigona postica. Micron. 33, 53–59PubMedCrossRefGoogle Scholar
Kirschvink, A.K., Gould, J.L. (1981) Biogenic magnetite as a basis for magnetic field detection in animals. Biosystems 13, 181–201PubMedCrossRefGoogle Scholar
Malone, L.A., Pham-Delegue, M.H. (2001) Effects of transgene products on honey bees (Apis mellifera) and bumblebees (Bombus sp.). Apidologie 32, 287–304CrossRefGoogle Scholar
Michelsen, A., Kirchner, W.H., Lindauer, M. (1986) Sound and vibrational signals in the dance language of the honeybee, Apis mellifera. Behav. Ecol. Sociobiol. 18, 207–212CrossRefGoogle Scholar
Navajas,
M., Migeon, A., Alaux, C., Martin-Magniette, M., Robinson, G., Evans,
J., Cros-Arteil, S., Crauser, D., Le Conte, Y. (2008) Differential gene
expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9, 301.PubMedCrossRefGoogle Scholar
Pierce,
A.L., Lewis, L.A., Schneider, S.S. (2007) The use of the vibration
signal and worker piping to influence queen behavior during swarming in
honey bees, Apis mellifera. Ethology 113, 267–275CrossRefGoogle Scholar
Pratt,
S.C., Kühnholz, S., Seeley, T.D., Weidenmüller, A. (1996) Worker piping
associated with foraging in undisturbed queenright colonies of honey
bees. Apidologie 27, 13–20CrossRefGoogle Scholar
Rangel, J., Seeley, T.D. (2008) The signals initiating the mass exodus of a honeybee swarm from its nest. Anim. Behav. 76, 1943–1952CrossRefGoogle Scholar
Schneider, S.S., Lewis, L.A. (2004) The vibration signal, modulatory communication and the organization of labor in honey bees, Apis mellifera. Apidologie 35, 117–131CrossRefGoogle Scholar
Seeley, T.D., Tautz, J. (2001) Worker piping in honey bee swarms and its role in preparing for liftoff. J. Comp. Physiol. A. 187, 667–676PubMedCrossRefGoogle Scholar
Stever H, Harst W, Kimmel S, Kuhn J, Otten C, Wunder B (2007) Change in behaviour of the honeybee Apis mellifera during electromagnetic exposure—follow-up study 2006 (Unpublished research report). http://agbi.uni-landau.de/material_download/elmagexp_bienen_06.pdf. Accessed 15 Sept 2009
Tautz, J. (2008) The buzz about bees: biology of a superorganism. Springer Verlag, BerlinCrossRefGoogle Scholar
Walker,
M.M., Bitterman, M.E. (1989a) Honeybees can be trained to respond to
very small changes in geomagnetic-field intensity. J. Exp. Biol. 145, 489–494Google Scholar
Walker, M.M., Bitterman, M.E. (1989b) Attached magnets impair magnetic-field discrimination by honeybees. J. Exp. Biol. 141, 447–451Google Scholar
Wenner, A.M. (1964) Sound communication in honeybees. Sci. Am. 210, 116–124Google Scholar
Wilson, W.T., Menapace, D.M. (1979) Disappearing disease of honey bees—survey of the United States. Am. Bee. J. 119, 184–186Google Scholar
Winston, M.L. (1991) The biology of the honey bee. Harvard University Press, CambridgeGoogle Scholar
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